Subcortical connectivity correlates selectively with attention’s effects on spatial choice bias

Abstract

Neural mechanisms of attention are extensively studied in the neocortex; comparatively little is known about how subcortical regions contribute to attention. The superior colliculus (SC) is an evolutionarily conserved, subcortical (midbrain) structure that has been implicated in controlling visuospatial attention. Yet how the SC contributes mechanistically to attention remains unknown. We investigated the role of the SC in attention, combining model-based psychophysics, diffusion imaging, and tractography in human participants. Specifically, we asked whether the SC contributes to enhancing sensitivity (d′) to attended information, or whether it contributes to biasing choices (criteria) in favor of attended information. We tested human participants on a multialternative change detection task, with endogenous spatial cueing, and quantified sensitivity and bias with a recently developed multidimensional signal detection model (m-ADC model). At baseline, sensitivity and bias exhibited complementary patterns of asymmetries across the visual hemifields: While sensitivity was consistently higher for detecting changes in the left hemifield, bias was higher for reporting changes in the right hemifield. Remarkably, white matter connectivity of the SC with the neocortex mirrored this pattern of asymmetries. Specifically, the asymmetry in SC–cortex connectivity correlated with the asymmetry in choice bias, but not in sensitivity. In addition, SC–cortex connectivity strength could predict cueing-induced modulation of bias, but not of sensitivity, across individuals. In summary, the SC may be a key node in an evolutionarily conserved network for controlling choice bias during visuospatial attention.